The Scientific Naturalist

Ecology, 100(12), 2019, e02818 © 2019 by the Ecological Society of America entirely benthic development (Ockelman 1958, Collin and Giribet 2010). The next question is, obviously: What makes it? Because the bivalve germinal epithelium has no secre- tory cells, and no auxiliary cells have been observed con- Cloaked bivalve oocytes: lessons in structing such a feature around developing oocytes, the evolution, ecology, and scientific most likely origin is the oocyte itself—and this has also been reported in unpublished work (cited in Gros et al. awareness 1997). Histological sections show a thin cloak around young oocytes (not shown), and a very thick one around 1 PETER G. BENINGER AND DAPHNE CHEREL mature oocytes (Fig. 1B). Manuscript received 20 March 2019; revised 15 May 2019; With respect to evolutionary lessons, coated oocytes accepted 17 June 2019. Corresponding Editor: John Pastor. have been observed in species from four of the six Faculte des Sciences, Universite de Nantes, 2 rue de la subclasses of the . There appears to be no Houssiniere, 44322 Nantes Cedex, France. taxonomic or evolutionary pattern in their occurrence; 1 E-mail: [email protected] they are found both in the primitive Cryptodonta and in the much later and Anomalodesmata Citation: Beninger, P. G., and D. Cherel. 2019. Cloaked (Table 1). In each of these subclasses, there are also bivalve oocytes: lessons in evolution, ecology, and scien- many species without coated oocytes, even within the tific awareness. Ecology 100(12):e02818. 10.1002/ecy.2818 same family (e.g., Pectinidae and Veneridae). The possi- bility that this is the result of multiple convergent evolu- Key words: bivalves; coat; mucopolysaccharides; oocytes; scien- tions of an identical character seems so remote as to be tific awareness. highly improbable. Conversely, if all bivalves possess the genetic and metabolomic equipment to produce such We have recently observed a gelatinous coat surround- coats (i.e., this is a pleisiomorphic character), why have ing the oocytes of Cerastoderma edule within which the so few such examples been observed? Assuming that it is development of early larval stages takes place (Fig. 1). a differentially expressed pleisiomorphic character, why Although variously coated oocytes are common in the is there no phylogenetic or taxonomic footprint? wider marine world, and among other molluscs, most If there is no phylogenetic relationship for the expres- bivalve researchers have never encountered such a thing. sion of this character, we might ask if there is an ecologi- And when they do, many simply ignore it, while others cal one. There is no indication that any ecological mislabel it as a “perivitelline space” (Gustafson and Reid parameter can switch this character on or off. All Ceras- 1986, Kandeel et al. 2013). Of course, the immediate toderma edule, as well as its sister species Cerastoderma question is: Why should we care? We should care first glaucum, present this character. Table 1 recapitulates because of the ecological and evolutionary lessons and some of the most important ecological parameters for perspectives this feature holds. And we should care marine bivalves: water temperature, depth, and habitat. because it tells us something very important about how Again, no pattern is evident; coated oocytes are found in the process of science funding can shape our view of the bivalves living at all temperatures, at all depths to the natural world. edge of the continental shelf, and in both epibenthic and First of all, what is this cloak? Of the few authors who endobenthic habitats. The endobenthic preponderance have actually reported its existence, most simply desig- of the 14 coated species is easily explained by the fact nate it as a “gelatinous covering” (Creek 1960), “jelly that the vast majority of all bivalve species are endoben- coat” (Hodgson and Burke 1988, Gros et al. 1997), or thic; similarly, the preponderance of reports from shal- “adhesive gelatinous egg capsule” (Gustafson and Lutz low depths probably represents material constraints: 1992). Unpublished data indicate that in orbicu- easily accessible bivalves are sampled more often than laris, the coat is composed of glycoproteins and proteo- those which require shipboard procedures. glycans (cited in Gros et al. 1997); this is consistent with Having ascertained that the presence of coated bivalve the staining we recently obtained using Alcian blue, and oocytes is not related to the major abiotic characteristics the lack of any periodic acid–Schiff staining in the com- of the marine habitat, we naturally proceed to question mon cockle, Cerastoderma edule (Fig. 1B). Although what selective advantage such a character might present. some bivalve species deposit gelatinous egg masses on We may set aside the possibility that the sheath con- the substratum, these are functionally and morphologi- tributes to the energy reserves necessary for the first cally different structures, characteristic of species with developmental stages, because it does not decrease in

Article e02818; page 1 Article e02818; page 2 THE SCIENTIFIC NATURALIST Ecology, Vol. 100, No. 12

in (A) (B)

ex c

n

nu hl p

5 mm 20 µm

(C) (D)

I d o c

c 20 µm 30 µm

FIG.1. Cerastoderma edule. (A) External view, showing both inhalant (in) and exhalant (ex) siphons. (B) Histological section of pedunculated (i.e., young) oocyte. Nucleus (n), nucleolus (nu), peduncle (p) and jelly coat (c) stained with Alcian blue, indicating acid mucopolysaccharides (AMPS). (C) Unstained, spawned oocyte surrounded by jelly coat (c). (D) Young larva (l, approx- imately 24 h in laboratory) developing within Alcian blue–stained jelly coat (c). Note adhering detritus particles (d). size over the course of larval development (Fig. 1C, D). mucopolysaccharide (AMPS) oocyte coat is Four alternative possibilities come to mind: undoubtedly resistant to digestion conditions (the intestine and stomach are themselves protected by a 1) Mechanical protection. Especially in the shallow coating of AMPS), such that even if swallowed, a fer- coastal habitats, currents can bring planktonic larvae tilized oocyte or larva may survive passage through into abrasive contact with topographic features. The the gut, as has been observed for copepod eggs sticky oocyte coat rapidly accumulates detrital parti- (Flinkman et al. 1994). cles (Fig. 1D), giving it a layer of nonliving protec- 4) Microbial protection—AMPS is well-known as both tion, supported by a shock-absorbing mucus layer. a physical and a chemical barrier to opportunistic 2) Predator protection. The 50-lm oocyte becomes a microorganisms (Romo et al. 2016), and the marine 200-lm spawned oocyte/larva once the mucus coat is environment is a veritable soup of hungry microor- fully hydrated (Fig. 1C, D), removing it from the ganisms. And finally, for spermatozoa which already prey size range of many copepods, which are the function at low Reynolds numbers (i.e., even swim- most numerous and voracious planktonic predators. ming in water is like swimming in honey for us), this Larger predators are fewer in number, further reduc- thick, viscous coat will impose severe challenges to ing predation pressure. In addition, the jelly coat successful fertilization, opening the possibility of itself, as well as the accumulated seston particles, sperm competition and sperm selection. may be unappealing or poorly recognized visually or olfactorily, resembling detritus or inorganic particu- The advantages provided by the jelly coat appear to be late matter rather than living food. substantial, but all biologists know that they must have 3) Postpredation protection. Many invertebrate oocytes a cost. Among the angles that could be investigated, are swallowed whole during spawns, for example, fecundity immediately comes to mind. The oocyte coat by fish (Fuiman et al. 2015). The acid occupies a very significant amount of space in the gonad December 2019 THE SCIENTIFIC NATURALIST Article e02818; page 3

TABLE 1. Occurrence of gelatinous oocyte coat among bivalve taxa, arranged from most primitive to most recent.

Habitat and Subclass Family species Cold Temp Warm Shallow Shelf Epi Endo References Protobranchia Solemyidae Solemya reidi 999Gustafson and Reid (1986) S. velum 99 9Gustafson and Lutz (1992) Pteriomorphia Pectinidae Chlamys hastata 999Hodgson and Burke (1988) Paleoheterodonta NR Heterodonta Astartidae Astarte sulcata 99 9 9 9Saleuddin (1965)† Cardiidae Cerastoderma 99 9Kingston (1974), glaucum Kandeel et al. (2013)† C. edule 99 9 9Creek (1960), present study Donacidae Dona9 vittatus 99 9Frenkiel and Mou€eza (1979) Lucinidae Lucinoma 99 9Gros et al. (1999) aequizonata Codakia 99 9Alatalo et al. orbicularis (1984); Gros et al. (1997) Thysasira gouldi 99999Blacknell and Ansell (1974) Semelidae Scrobicularia 99 9Frenkiel and plana Mou€eza (1979) Veneridae Mercenaria 99 9 9 9Loosanoff and mercenaria Davis (1950) M. camechiensis 99 9Loosanoff and Davis (1963) Venus striatula 99 9 9 9Ansell (1961) Arcticidae Arctica islandica 999Lutz et al. (1982) Anomalodesmata Laternulidae Laternula 999Ansell and Harvey elliptica (1997); Peck et al. (2007) Pandoridae Pandora 99 9 99Allen (1961) inaequivalvis

Note: Epi, epibenthic; Endo, endobenthic; NR, none reported to date; Temp, temperate; Shelf, found over the depth range of the continental shelf. † Not reporzted, but visible in drawings/micrographs.

acinus, which could otherwise be occupied by more that nobody works for free (not counting the overtime oocytes. Do species with coated oocytes produce fewer scientists put in!), it is obvious that it is usually the oocytes annually than species with uncoated oocytes, or species for which a budget has been allocated that do they compensate for fewer oocytes by having longer will be studied. A quick check of published papers on spawning periods? Larval survival is another obvious bivalve biology will show that an overwhelming research tack. Does the oocyte coat reduce larval mor- majority concern the few species that support major tality, especially in the early, essentially endotrophic fishery and/or aquaculture industries. As it happens, stages? Energetics is also an interesting angle—How none of them have been reported to have coated much of the total reproductive production budget does oocytes. A lack of major commercial importance is oocyte coating represent? And finally, one is left with a typical of the 17 species in which individually coated sense of awe that a feature such as this could be either oocytes (as opposed to benthic egg masses) have been switched on or off, species by species, in so many dis- observed to date (Table 1). The result is that most tantly and closely related taxa. bivalve biologists, working on the high-profile (and Perhaps the most interesting lesson provided by comparatively well-funded) major commercial species, bivalve coated oocytes is in what they tell us about have no idea that coated bivalve oocytes exist. The the way we conduct science itself. Just as it is obvious specialists have a blinkered view of their subject. Article e02818; page 4 THE SCIENTIFIC NATURALIST Ecology, Vol. 100, No. 12

There may be many more bivalve species with coated Fuiman, L. A., T. L. Connelly, S. K. Lowerre-Barbieri, and J. oocytes out there. As long as marine bivalve researchers W. McClelland. 2015. Egg boons: central components of mar- – focus preponderantly on the high-profile commercial ine fatty acid food webs. Ecology 96:362 372. Gros, O., L. Frenkiel, and M. Mou€eza. 1997. Embryonic, larval, species, we will simply continue not to assimilate this and post-larval development in the symbiotic clam Codakia basic fact into our scientific consciousness. Ignoring the orbicularis (Bivalvia: Lucinidae). Invertebrate Biology existence of these oocytes not only ignores the phe- 116:86–101. nomenon, but also closes to scientific inquiry all of the Gros, O., M. R. Duplessis, and H. Felbeck. 1999. Embryonic fascinating questions it raises. It is likely that many simi- development and endosymbiont transmission mode in the lar situations exist with respect to orphan taxa, and, symbiotic clam Lucinoma aequizonata (Bivalvia: Lucinidae). – more generally, orphan scientific questions. Invertebrate Reproduction and Development 36:93 103. Gustafson, R. G., and R. A. Lutz. 1992. Larval and early post- ACKNOWLEDGMENTS larval development of the protobranch bivalve Solemya velum (: Bivalvia). Journal of the Marine Biological Asso- We thank Professor John Pastor for his helpful text sugges- ciation of the United Kingdom 72:383–402. tions, as well as two anonymous reviewers for their constructive Gustafson, R. G., and R. G. B. Reid. 1986. Development of the comments. Underscoring a key point in this paper, no funding pericalymma larva of Solemya reidi (Bivalvia: Cryptodonta: was provided for this work. Solemyidae) as revealed by light and electron microscopy. Marine Biology 93:411–427. Hodgson, C. A., and R. D. Burke. 1988. Development and lar- LITERATURE CITED val morphology of the spiny scallop, Chlamys hastata. Biolog- – Alatalo, P., C. J. Berg, Jr., and C. N. D’Asaro. 1984. Reproduc- ical Bulletin 174:303 318. tion and development in the lucinid clam Kandeel, K. E., S. Z. Mohammed, A. M. Mostafa, and M. E. (Linne, 1758). Bulletin of Marine Science 34:424–434. Abd-Allaa. 2013. Reproductive biology of the cockle Cerasto- Allen, J. A. 1961. The development of Pandora inaequivalvis derma glaucum (Bivalvia: Cardiidae) from Lake Qarun, – (Linne). Journal of Embryology and Experimental Morphol- Egypt. Egyptian Journal of Aquatic Research 39:249 260. ogy 9(Part 2):252–268. Kingston, P. F. 1974. Studies on the reproductive cycles of Car- – Ansell, A. D. 1961. Reproduction, growth and mortality of dium edule and C. glaucum. Marine Biology 28:317 323. Venus striatula (Da Costa) in Kames Bay, Millport. Journal Loosanoff, V. L., and H. C. Davis. 1950. Conditioning V. merce- of the Marine Biological Association of the United Kingdom naria for spawning in winter and breeding its larvae in the – 41:191–215. laboratory. Biological Bulletin 98:60 65. Ansell, A. D., and R. Harvey. 1997. Protected larval develop- Loosanoff, V. L., and H. C. Davis. 1963. Rearing of bivalve – ment in the Antarctic bivalve Laternula elliptica (King and mollusks. Advances in Marine Biology 1:1 136. Broderip) (Anomalodesmata: Laternulidae). Journal of Mol- Lutz, R. A., R. Mann, J. G. Goodsell, and M. Castagna. 1982. luscan Studies 63:285–286. Larval and early post-larval development of Arctica islandica. Blacknell, W. M., and A. D. Ansell. 1974. The direct develop- Journal of the Marine Biological Association of the United – ment of gouldi (Phillipi). Thalassia Jugoslavica Kingdom 62:745 769. 10:23–43. Ockelman, W. K. 1958. The zoology of east Greenland marine ø ø Collin, R., and G. Giribet. 2010. Report of a cohesive gelati- Lamellibranchiata, Meddelelser om Gr nland, Gr nland. nous egg mass produced by a tropical marine bivalve. Inverte- Peck, L. S., D. K. Powell, and P. A. Tyler. 2007. Very slow devel- brate Biology 129:165–171. opment in two Antarctic bivalve molluscs, the infaunal clam Creek, G. A. 1960. The development of the Lamellibranch Car- Laternula elliptica and the scallop Adamussium colbecki. Mar- – ine Biology 150:1191–1197. dium edule L. Journal of Zoology 135:243 260. Flinkman, J., I. Vuorinen, and M. Christiansen. 1994. Calanoid Romo,M.R.,D.Perez-Martınez,andC.C.Ferrer.2016.Innate – copepod eggs survive passage through fish digestive tracts. immunity in vertebrates: an overview. Immunology 148:125 139. ICES Journal of Marine Science 5:127–129. Saleuddin, A. S. M. 1965. The mode of life and functional anat- Frenkiel, L., and M. Mou€eza. 1979. Developpement larvaire de omy of Astarte spp. (Eulamellibranchia). Journal of Mollus- – deux Tellinacea, Scrobicularia plana (Semelidae) et Donax vit- can Studies 36:229 257. tatus (Donacidae). Marine Biology 55:187–195.